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The Restriction of the Heart Morphogenetic Field in Xenopus Levis

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The Restriction of the Heart Morphogenetic Field in Xenopus Levis DEVELOPMENTAL BIOLOGY 140,328-336 (1990) The Restriction of the Heart Morphogenetic Field in Xenopus Levis AMY K. SATER’ AND ANTONE G. JACOBSON Department of Zoology, Center for Devebpmental Biology, University of Texas, Austin, Texa.s 78712 Accepted April 12, 1990 We have examined the spatial restriction of heart-forming potency in Xenopus 1ueG.sembryos, using an assay system in which explants or explant recombinates are cultured in hanging drops and scored for the formation of a beating heart. At the end of neurulation at stage 20, the heart morphogenetic field, i.e., the area that is capable of heart formation when cultured in isolation, includes anterior ventral and ventrolateral mesoderm. This area of developmental potency does not extend into more posterior regions. Between postneurula stage 23 and the onset of heart morphogenesis at stage 28, the heart morphogenetic field becomes spatially restricted to the anterior ventral region. The restriction of the heart morphogenetic field during postneurula stages results from a loss of developmental potency in the lateral mesoderm, rather than from ventrally directed morphogenetic movements of the lateral mesoderm. This loss of potency is not due to the inhibition of heart formation by migrating neural crest cells. During postneurula stages, tissue interactions between the lateral mesoderm and the underlying anterior endoderm support the heart-forming potency in the lateral mesoderm. The lateral mesoderm loses the ability to respond to this tissue interaction by stages 27-28. We speculate that either formation of the third pharyngeal pouch during stages 23-27 or lateral inhibition by ventral mesoderm may contribute to the spatial restriction of the heart morphogenetic field. o 1990 Academic PWSS. IW. INTRODUCTION stages also contribute to heart formation (Ekman, 1921; Humphrey, 1972). These earlier studies included hetero- Many events of pattern formation and organogenesis topic transplantations (Copenhaver, 1924; Ekman, 1925) are mediated by inductive interactions that establish to measure the spatial extent of heart-forming potency regions of developmental potency, known as morphoge- during postneurula stages. In these experiments, the netic fields. A morphogenetic field generally comprises presumptive heart mesoderm was removed from the an- both the area of tissue that is fated to develop into a terior ventral region and replaced with grafts of meso- given structure during normal development and the tis- derm from more lateral or more posterior regions. sue immediately surrounding this area, which is capable Heart formation by the grafted tissue was interpreted of developing into the given structure under experimen- as an indicator that the grafted tissue was able to re- tal conditions (Jacobson and Sater, 1988). Extensive ex- spond to continued inductive signals. In addition, extir- perimental analysis by a number of workers has shown pation experiments measured the ability of the that the spatial extent of a morphogenetic field de- surrounding tissues to undergo regulative replacement creases with time, as the developmental potency re- in the absence of the presumptive heart mesoderm (Co- quired to make a given organ or structure is lost from penhaver, 1924). Again, cases of heart formation by the peripheral regions of the field. While the inductive in- surrounding tissues were thought to result from contin- teractions responsible for the establishment of morpho- ued induction by the underlying endoderm. Thus, earlier genetic fields have received considerable attention, the investigators often regarded tissue interactions during mechanisms underlying the spatial and temporal regula- postneurula stages as responsible for the initial estab- tion of developmental potency during subsequent devel- lishment of heart-forming potency; the induction of opment are completely unknown. heart formation during gastrula or neurula stages went We have previously shown that the inductive interac- unrecognized. tions responsible for the specification of heart meso- Tissue interactions during postneurula stages may derm occur during gastrulation in Xenopus laevis (Sater regulate the spatial extent of heart-forming potency, and Jacobson, 1989). A number of findings suggest that i.e., the heart morphogenetic field, which is induced ear- tissue interactions during neurula and postneurula lier in development. In the following experiments, we have used heart formation in explants as an assay to 1 Present address: Department of Molecular and Cell Biology, Divi- measure the spatial extent of the heart morphogenetic sion of Cell and Developmental Biology, University of California, field in postneurula-stage Xenoms embryos. These stud- Berkeley, CA 94720. ies were undertaken in order to examine the tissue in- 0012-1606/90 $3.00 328 Copyright 0 1990 by Academic Press, Inc. All rights of reproduction in any form reserved. SATERANDJACOBSON Xenopus Heart Mwphogenetic Field 329 teractions governing the maintenance and restriction of 23°C). Explants and explant recombinates were cul- the heart morphogenetic field. tured in hanging drops of Niu-Twitty solution contain- ing 50 III/ml penicillin and 50 mg/ml streptomycin MATERIALS AND METHODS (Niu-Twitty plus pen/strep) at 17”C, as described in Sater and Jacobson (1989). Grafts of embryonic tissue Embryos were allowed to heal in Niu-Twitty solution plus pen/ Embryos were obtained from both natural matings strep for up to 1 hr at 23°C; they were subsequently and in vitro fertilization. Adult Xenop were induced to maintained at 17°C. mate by a series of injections of human chorionic gonad- otropin (HCG; Sigma Chemicals, St. Louis, MO), accord- Microinjection of Lineage Tracer ing to the following schedule: males were given two in- Prior to first cleavage, embryos were transferred to jections of 150 International Units (IU) of HCG 32 and 8 5% Ficoll (Sigma) in 33% MR; embryos were then pres- hr before they were placed in the mating tank; females sure-injected with approximately 3 nl of 50 mg/ml were given one injection of 250 IU HCG 8 hr before and fluoresceinated dextran-amine (FDA) (Sigma) in dis- one injection of 500 IU HCG immediately before they tilled water, resulting in a final concentration of approx- were placed in the mating tank. Frogs were allowed to imately 150 rig/embryo. Micropipets with an external mate overnight. The following morning, embryos were tip diameter of 20-25 pm were prepared by pulling boro- collected and dejellied for 5 min in 2% cysteine HCl, pH silicate glass microcapillary tubes on a Brown-Flaming 7.4. Dejellied embryos were washed extensively in 10% electrode puller (Sutter Instruments, San Francisco, Holtfreter’s solution (Jacobson, 1966) and maintained in CA). Micropipets were calibrated by expelling FDA into 10% Holtfreter’s solution at 1’7°C. All embryos were a drop of mineral oil and measuring the diameter of the staged according to Nieuwkoop and Faber (1967). expelled FDA. Following microinjection, embryos were In vitro fertilizations were carried out by the methods allowed to heal in 33% MR containing 5% Ficoll. Em- of Gimlich and Gerhart (1984). Ovulation was induced bryos that leaked cytoplasm were discarded. by an injection of 500 IU HCG (Sigma). Approximately 12 hr later, oocytes were stripped into a petri dish con- Histology taining minced testis tissue in a minimal volume of 33% modified amphibian Ringer (MR; 100% MR: 0.1 MNaCl, Embryos containing grafts of FDA-labeled tissue 2 mM KCl, 2 mM CaCl,-2H,O, 1 mM MgCl,-GH,O, buff- were fixed in freshly prepared 2% paraformaldehyde in ered to pH 7.4 with NaHCO,) (Gimlich and Gerhart, 0.1 M Na cacodylate, pH 7.4, for approximately 20 hr at 1984). Oocytes and sperm were mixed gently by rotating 6°C. Embryos were then washed 15-24 hr in 0.1 M Na the dish and then allowed to stand for several minutes cacodylate, pH 7.4, at 6°C. Embryos were dehydrated so that fertilization could occur. Oocytes were then de- through an ethanol-butanol series, embedded in Para- jellied as described earlier and maintained in 33% MR plast, and sectioned at 8 pm. Sections were collected on at 17°C. gelatin-coated slides, dewaxed through a xylene-eth- anol series, and mounted in 80% glycerol containing 4% N-propyl gallate (Sigma; Gimlich and Braun, 1985). Microsurgery and Culture of Explants and Sections were viewed using epifluorescence optics Explant Recombinates (Zeiss). For microsurgery, embryos were transferred to petri dishes containing sterile, freshly prepared Niu-Twitty RESULTS solution over a cushion of 2% agar. All embryonic oper- The Heart Mvhogenetic Field at the End ations were performed using electrolytically sharpened of Neurulation tungsten needles, sharpened watchmaker’s forceps, and eyebrow hair knives. Operations involving the separa- At the end of neurulation (stage 20), the two regions tion of mesoderm and endoderm were performed in Niu- of prospective heart mesoderm, which originally lay at Twitty solution containing 0.01% trypsin (Sigma Type the anterior lateral edge of the mesodermal mantle, IX), as described by Slack (1984). Explants isolated in have migrated ventrally to fuse at the ventral midline in the presence of trypsin were subsequently incubated in the anterior region (Nieuwkoop and Faber, 1967). Thus, 0.02% soybean trypsin inhibitor (SBTI; Sigma Type II- by stage 20, the prospective heart mesoderm has arrived S) in Niu-Twitty solution for several minutes before at the site of heart morphogenesis and undergoes no they were placed in culture. Explant recombinates were further large-scale movements. A crude map of the allowed to heal in Niu-Twitty solution containing SBTI heart morphogenetic field at this stage was constructed for up to 1 hr at room temperature (approximately by culturing ventral and lateral explants from anterior, DEVELOPMENTALBIOLOGY VOLUME 140,1990 vesicles, which were examined with a dissecting micro- scope. Within 3 to 4 days after explantation, explants became inflated and translucent; explants were subse- quently examined with a compound microscope and transmitted light. Explants isolated from ventral re- gions always exhibited large, well-developed hearts, which appeared within 5 days after explantation.
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